Barriers and facilitators to access and uptake of intermittent preventive treatment with sulfadoxine-pyrimethamine among pregnant women in Nigeria: a scoping review

Background Malaria in pregnancy is a significant public health concern in Nigeria. It threatens pregnant women and their unborn babies and undermines the achievement of Sustainable Development Goal 3. The World Health Organization has recommended intermittent preventive treatment with sulfadoxine-pyrimethamine [IPTp-SP] for its control, but there are challenges to its access and uptake. Methods Using the Arksey and O'Malley framework and the cascade of care model, we conducted a scoping review to investigate barriers and facilitators of IPTp-SP access and uptake, including their influence on pregnant women's health-seeking behaviour for the control of malaria in pregnancy in Nigeria. We searched seven scientific databases for papers published from 2005 to date. Results We included a total of 31 out of 2149 articles in the review. Poor provider knowledge of the IPTp-SP protocol and lack of essential commodities for sulphadoxine-pyrimethamine administration in clinics are significant barriers to IPTp-SP use. Staff shortages and poor remuneration of health care professionals are obstacles to IPTp-SP utilisation. Conclusions To improve IPTp-SP access and uptake, the government should ensure a continuous supply to clinics and support the employment of additional health care professionals who should be well paid and trained on using the IPTp-SP protocol.


INTRODUCTION
Malaria in pregnancy [MiP] is one of the major causes of maternal mortality and adverse pregnancy outcomes in Nigeria. It undermines the achievement of Sustainable Development Goal 3, which targets maternal mortality reduction and malaria eradication by 2030 [1][2][3]. Fortunately, chemoprophylaxis can help to prevent MiP [1]. The World Health Organization (WHO) recommends that all pregnant women in malaria-endemic areas receive at least three rounds of intermittent preventive treatment with sulfadoxine-pyrimethamine (IPTp-SP) for MiP control. Despite adopting this guideline, the uptake of IPTp-SP among pregnant women in many African countries remains very low [4,5].
The Federal Ministry of Health in Nigeria introduced the IPTp-SP strategy in 2005. As a preventative treatment, IPTp-SP is given to pregnant women, whether they have malaria or not, at monthly intervals from the second trimester until delivery. Under the national protocol, IPTp-SP is offered free as a directly observed treatment (DOT) through ante-natal clinics (ANCs) in public hospitals and non-governmental organisation facilities [6][7][8].
However, challenges at all levels of the health system, including macro-level issues and supply and demand issues, limit the effectiveness of this policy [1,5,9,10] and impede the progress on MiP control in Nigeria. The percentage of women who receive one IPTp-SP round has increased steadily since 2014, but uptake of two and three rounds remains low [11]. In 2018, Nigeria had one of the highest occurrences of MiP, but less than 25% of ANC attendees completed the recommended three rounds [7,12]. With about 90% of Nigeria's 7.5 million pregnant women being at risk of getting malaria annually [1,13], an incomplete course of IPTp-SP can have severe consequences for women and their babies. Malaria accounts for almost 50% of the diseases and for 15% of anaemia reported among pregnant women in Nigerian hospitals. Reports of morbidity and mortality among pregnant women due to this disease are estimated to be 70.5% and 11%, respectively. Among neonates, the incidence of between 5-14% low birth weight (LBW) and about 30% preventable LBW is attributed to MiP [2,5,10,[14][15][16][17][18][19]. The failure to achieve broad coverage of IPTp-SP among pregnant women reflects the acknowledgement of a gap between an available policy and the barriers to its implementation.
IPTp-SP acceptance and coverage have been an investigation target for over ten years [4,[20][21][22]. However, to the best of our knowledge, no single review focussing on Nigeria has been conducted. Using elements of the Cascade of Care model (CoC), this study examined the barriers and facilitators of IPTp-SP access and uptake, including their influence on pregnant women's health-seeking behaviour for MiP control in Nigeria. The CoC, which has been used successfully in chronic communicable and non-communicable disease programmes [23][24][25][26], describes the care-seeking steps of patients from diagnosis to treatment. It helps to analyse patients' progress towards achieving better health outcomes and tackling any identified potential barriers to seeking care [27]. The CoC is a valuable framework for exploring the obstacles and facilitators along the pathway of IPTp-SP utilisation for MiP control. We anticipate that the study findings will inform future research into the challenges facing IPTp-SP coverage and improve its utilisation across Nigeria.

MATERIALS AND METHODS
We used the Arksey and O'Malley [28] methodological framework and the Preferred Reporting Items for Systematic Reviews and Meta-Analyses extension for Scoping Reviews (PRISMA-ScR) checklist by Tricco et al. [29] (see checklist in Appendix A). A five-stage process was used: (1) identifying the research question, (2) identifying relevant studies, (3) study selection, (4) charting the data, and (5) collating, summarising and reporting results [28]. A scoping review protocol was created and is available upon request.
This review adapted the CoC model with the following key stages: (a) a woman is diagnosed with pregnancy, (b) pregnant woman registers in an ANC and attends ANC regularly, (c) pregnant woman takes IPTp-SP at least three times during pregnancy.
This pathway shows that upon becoming pregnant, women should register in and be consistent with ANC visits to get the three or more IPTp-SP rounds required to protect them from MiP. However, several barriers along this pathway span throughout and beyond the health system, including individual and interpersonal factors.

Identifying the research question
This review was guided by the research question: "What are the barriers and facilitators to IPTp-SP utilisation, and their influence on the health-seeking behaviour for the control of MiP among pregnant women in Nigeria?".

Identifying relevant studies
We developed search strategies in collaboration with an experienced librarian at a post-secondary institution. Seven databases were searched through CINAHL, Embase, Web of Science, MEDLINE, Global Health, JSTOR, and Malaria in Pregnancy. The search was limited to English language articles because of the language skills of team members and to publications from 2005 to the present because the IPTp-SP policy was adopted in Nigeria that same year. The searches were conducted from January to March 2021, with the most recent search executed on March 20, 2021. See Appendix B for the complete search strategies.

Inclusion and exclusion criteria
We included articles focused on IPTp-SP access, coverage, uptake, barriers, facilitators, and utilisation in Nigeria. Books or chapters and articles focused on other antimalarials, children and infants, HIV positive and sickle cell anaemic pregnant women were excluded.

Study selection
Two reviewers (PO and HC) screened the study titles, abstracts, and full texts using Covidence, a web-based reviewing platform. The two reviewers discussed disagreement about study eligibility until consensus.

Charting the data
A charting template, shown in Table 1, was used to record relevant information from included articles [30].

RESULTS
A total of 2149 articles were exported to Covidence. After duplicates were removed, the titles and abstracts of 1145 articles were screened. Next, 316 fulltext articles were screened, and 31 studies were included in the review ( Figure 1). Articles were excluded during the full-text screening phase for the following reasons: • Non-availability of the full text. • The studies focused on populations other than pregnant women. • Another source better covers information.
• Studies covered sub-Saharan African countries other than Nigeria. The adapted CoC model was used to categorise and examine the barriers and facilitators of IPTp-SP access and uptake in the literature ( Figure 2).

Woman diagnosed with pregnancy
In this phase, individual-level factors such as perception about pregnancy and poor knowledge of IPTp-SP act as barriers to IPTp-SP utilisation.
Generally, pregnancy is seen as a regular occurrence and not an illness. While this is correct, it prevents pregnant women and their spouses from accepting medical interventions like IPTp-SP [31]. People also consider some malaria symptoms like high fever and general weakness typical pregnancy signs. This belief affects care-seeking behaviour for the control and treatment of MiP [32].
Similarly, poor knowledge of IPTp-SP prevents pregnant women from requesting SP in clinics; furthermore, in instances where they get the drug outside the hospital, it may be inappropriately used [33,34]. Many pregnant women report that ANC providers do not give enough details about IPTp-SP, including the required dose and timing, benefits, or why it is important in pregnancy. Some women refuse the treatment, thinking that only individuals with malaria should take IPTp-SP [2,7,[35][36][37].

Pregnant woman registers in an ANC and attends ANC regularly
After pregnancy confirmation, a woman should register in an ANC where IPTp-SP is prescribed and administered. However, individual, interpersonal, and health system factors impede IPTp-SP utilisation.  [38][39][40][41]. Within the Nigerian culture, women lack the autonomy to make healthrelated decisions independent of their husbands and sometimes sisters and mothers-in-law. There have been reports of women not attending ANC or taking IPTp-SP because their spouses did not consent [2,7,10,31,33,36]. Some men discourage ANC visits because of cost, while others do so because they prefer traditional birth attendants (TBAs) [31]. Delays and the negative attitude of healthcare professionals (HCPs) discourage pregnant women from regularly attending ANC, especially in public hospitals where they can obtain free SP [7,31]. They explore other options, including self-medication with herbal mixtures and unprescribed antimalarials, and seek treatment from traditional and faith homes, where they claim to be respectfully treated [7,31,32]. The unfriendliness of HCPs has been attributed to lack of job satisfaction, low remuneration, poor work environment, and excess workload; however, long wait times are attributed to understaffing [1,31,42].
Facilitators of IPTp-SP utilization include employment status, wealth index, and level of education. Gainfully employed pregnant women and those in the higher wealth index are more likely to register in an ANC and utilise IPTp-SP because they can make financial and health-related decisions independent of their spouses [1,10,38,39,[43][44][45].  Similarly, pregnant women who are educated and have educated spouses are more likely to attend ANC and use IPTp-SP. Education has been shown to enhance pregnant women's understanding of the adverse effects of malaria and the importance of its preventive strategies [36,38,40,[44][45][46].

Pregnant woman takes IPTp-SP at least three times during pregnancy
HCP unawareness of the availability and implementation of the IPTp-SP protocol is a challenge at this stage of the cascade. Some private hospitals do not have this protocol as part of their treatment policy [2,19,22,37,[47][48][49][50]. Physicians still prescribe the weekly regimen of chloroquine and pyrimethamine despite their reduced potency and poor compliance among pregnant women. Reasons cited for this prescription style are the affordability and accessibility of other antimalarials and poor knowledge of drug resistance patterns among physicians [6,22,31,47,50]. Only a few HCPs, mostly in public hospitals, know the IPTp-SP protocol, but there is confusion regarding dose, timing, and the gestational age to commence treatment. Insufficient training and supervision of HCPs are highlighted as reasons for this poor understanding [2,19,22,[48][49][50]. Furthermore, some pregnant women refrain from IPTp-SP because they think it could cause harm, especially in the second and third trimesters. They report that the drug weakens them and associate its use with frequent urination and adverse outcomes like skin reactions, abortions, and foetal abnormalities. Some women consider taking SP a waste of time because they doubt its efficacy [2,7,20,34,37,51]. Others refuse because the drug is unfamiliar, and their husbands did not buy it. This shows a distrust for HCPs which may be linked to previous rumours in the region about how vaccines were reportedly fortified with anti-fertility drugs to prevent conception [31,36].
Under the IPTp-SP scheme in Nigeria, SP is free as it is supplied to public clinics by the government. Unfortunately, this drug is frequently unavailable because the government fails to ensure its constant supply [19,20,31]. Pregnant women either are turned away without receiving IPTp-SP or are asked to pay for it. Prescription notes are sometimes given to pregnant women to buy the drug from pharmacies without the assurance that the right medicine will be purchased or used appropriately [2,7]. User fees impose additional costs on pregnant women, who are usually disappointed and often refuse to buy SP because they know it should be free [19,49]. Unavailability of potable water and clean cups to administer SP as a directly observed treatment (DOT) and inadequate staff to monitor pregnant women taking the drug also limit pregnant women's uptake of complete IPTp-SP rounds [19,35,39,49]. Other issues include HCP unawareness of IPTp-SP as a DOT and the safety of using SP without food. Some HCPs have told pregnant women to use SP at home after meals, unknowingly giving these women the opportunity to default with drug uptake [33,49]. Further, despite the convergence of evidence demonstrating the benefits and safety of using IPTp-SP, some HCPs in Nigeria still think contrarily. Consequently, HCPs minimally prescribe IPTp-SP, preventing pregnant women from taking at least three rounds of IPTp-SP [4,7,37,44,[48][49][50].
Facilitators in this phase are the use of government hospitals and geographical locations. Government hospitals have reported increased IPTp-SP utilisation due to HCPs educating ANC attendees about the benefits [6,10,43]. Making SP available free of charge in government hospitals also increases IPTp-SP uptake [6,10,43,47]. Adeola and Okwilagwe [10] discovered that rural pregnant women are better users of IPTp-SP than their urban counterparts. Their receptiveness may be connected to the Rollback Malaria [RBM] programme, which enhances IPTp-SP prescription and focuses more on rural communities in Nigeria. Anecdotal evidence suggests that urban dwellers make minimal effort to prevent MiP because they see it as a common disease [10]. Contrastingly, Ndu et al. [43] and Olugbade et al. [44] posit that urban pregnant women are better users of IPTp-SP because they can easily access service providers and current information from the media. Oyefabi et al. [19] found that IPTp-SP is more readily available in urban health centres. More research needs to be done to resolve these contrasting views.

DISCUSSION
Despite the availability of a clear policy and the known effectiveness of IPTp-SP in preventing MiP, uptake and completion of the recommended dose by pregnant women remains very low [1]. Most barriers to IPTp-SP utilisation are within the health system, but individual and interpersonal factors are also significant obstacles [1,2,4,52]. Our study highlights the interconnection between the health system, individual, and interpersonal barriers and their influence on one another. For example, frequent SP shortage has resulted in the introduction of user fees (health system factors), which discourages pregnant women from attending ANCs (individual factor) and encourages their loss of trust in HCPs (interpersonal factor) because they know SP should be free [31,32,49].
For IPTp-SP utilisation to improve in Nigeria, gaps within the health system must be addressed [1]. First, the government must provide continuous training for all HCPs regarding the IPTp-SP protocol to improve their knowledge of its benefits, reduce their concerns about risks, and encourage its prescription. Second, supportive supervision of HCPs by credible peers is needed to promote IPTp-SP policy implementation and guarantee proper quality assurance and monitoring, ultimately improving IPTp-SP utilisation [1,4,53]. Third, increased government commitment towards providing SP, potable drinking water, and clean cups is required and has been shown to increase IPTp-SP coverage and uptake in other countries, including Zambia and Senegal [4,53,54]. There are also records of how these approaches have eliminated SP user fees and enhanced HCP adherence to the DOTs strategy recommended for IPTp-SP administration [2,19,20,31,33,35,39,49,55].
The encouragement of HCPs is likewise vital [1]. Many HCPs in Nigeria are dissatisfied with their jobs and limited career development opportunities. They are also overworked and inadequately remunerated [1,7,31,42]. Studies have found that overworked and underpaid staff may be hostile towards clients, and this hostility negatively influences clients' health-seeking behaviour [42,53]. Efforts should be made to hire more HCPs, increase their pay, and provide career enhancement and educational opportunities.
Individual factors also need to be addressed. Pregnant women's poor knowledge and understanding of the use and benefits of IPTp-SP affect their perception of IPTp-SP safety and efficacy, erroneously linking its use to abortion. This flawed perception often prevents pregnant women from demanding and using the drug [2,7,[34][35][36][37]51,55]. While mild and brief side effects like nausea, vomiting, and dizziness may occur when using SP the first time, this drug is generally well tolerated [56]. Health education can increase uptake by enhancing understanding of the benefits and safety of SP and correcting some of the misconceptions about pregnancy that prevent pregnant women from accepting medical interventions [2,4].
Considering the success of community mobilisation with the onchocerciasis control programme in Uganda, a similar strategy may be effective for promoting and augmenting ANC attendance and IPTp-SP utilisation [2,4,53]. A community mobilisation effort involves pregnant women's access to SP, frequent personalised health education, follow-up visits and reminders from Community Directed Distributors (CDD), even when they miss ANC. This programme does not undermine ANC attendance because the CDDs are trained to refer pregnant women to hospitals for complete ANC services [2,53,57,58]. This cost-effective and feasible strategy has demonstrated positive results in studies in Uganda [59,60]. In addition, employing a group ANC service delivery model could encourage more robust peer support for and administration of IPTp-SP through increased ANC visits [61].
The interpersonal factor of cultures is a challenge because it is a way of life passed down through generations and is difficult to change. Since the Nigerian culture supports that men make health-related decisions for their pregnant wives, a practical approach may be to educate these men on the dangers of MiP and the benefits of IPTp-SP [4,31,36]. Traditional and faith-based providers should receive similar education and training, as some women are permitted to seek ANC services only from these groups. Adequate knowledge of MiP, IPTp-SP use, and where it can be accessed can encourage traditional birth attendants and faithbased providers to refer their clients to public hospitals for MiP control [7]. Regarding pregnant women's lack of trust in HCPs and men discouraging their wives from ANC visits because of SP payment, eradication of user fees through constant SP availability may resolve this [4,53]. Finally, training HCPs to provide customer service respectfully may increase the likelihood that pregnant women will comply with IPTp-SP uptake in clinics [31,53].

RECOMMENDATIONS
A comprehensive approach is required to overcome barriers and mitigate their individual and collective impact. It is recommended that user fees be eliminated through regular SP availability and that HCP understanding of adherence to the national IPTp-SP protocol is increased [2,19,20,31,33,35,39,49,55]. Hiring more HCPs can also help to alleviate their stress and reduce their hostility toward their patients. Furthermore, the distribution of SP should not be limited to clinics but should be offered to pregnant women in the community. This approach can reach women, particularly those in rural areas, who do not visit the ANC during their pregnancy [20, 57,58]. Finally, adopting a group antenatal clinic service approach may give pregnant women the opportunity to build social support, encouraging IPTp-SP use [61,62].

LIMITATIONS
Only one reviewer extracted data. However, two reviewers screened and identified relevant studies using pre-determined inclusion and exclusion criteria to minimise error. Due to financial and time constraints, grey literature and consultation with key stakeholders were excluded despite being suggested by the framework used [28]. Although the literature search was limited to English articles, the diversity of journals included contributes to the strength of the review.

CONCLUSION
This review has shown how barriers at the individual, interpersonal, and health system levels affect implementing the IPTp-SP policy and its uptake. If Nigeria is to achieve SDG3 and reach the muchdesired reduction in MiP burden, the identified bottlenecks must be tackled. The review highlights the need for increased government involvement and investments in hiring, training, and financially supporting HCPs. The availability of tools for IPTp-SP administration in clinics should also be ensured. Most of the papers included in this review focused on health system barriers to the uptake of IPTp-SP, making it apparent that there is a lack of studies on how factors within the community influence IPTp-SP uptake among pregnant women in Nigeria. Further research is therefore needed to understand how community-level contextual factors influence pregnant women's uptake of recommended IPTp-SP doses.

Summary of evidence
24 Summarize the main results (including an overview of concepts, themes, and types of evidence available), link to the review questions and objectives, and consider the relevance to key groups.

5-6
Limitations 25 Discuss the limitations of the scoping review process. 7 Conclusions 26 Provide a general interpretation of the results with respect to the review questions and objectives, as well as potential implications and/or next steps.